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1.  Visual-auditory integration for visual search: a behavioral study in barn owls 
Barn owls are nocturnal predators that rely on both vision and hearing for survival. The optic tectum of barn owls, a midbrain structure involved in selective attention, has been used as a model for studying visual-auditory integration at the neuronal level. However, behavioral data on visual-auditory integration in barn owls are lacking. The goal of this study was to examine if the integration of visual and auditory signals contributes to the process of guiding attention toward salient stimuli. We attached miniature wireless video cameras on barn owls’ heads (OwlCam) to track their target of gaze. We first provide evidence that the area centralis (a retinal area with a maximal density of photoreceptors) is used as a functional fovea in barn owls. Thus, by mapping the projection of the area centralis on the OwlCam’s video frame, it is possible to extract the target of gaze. For the experiment, owls were positioned on a high perch and four food items were scattered in a large arena on the floor. In addition, a hidden loudspeaker was positioned in the arena. The positions of the food items and speaker were changed every session. Video sequences from the OwlCam were saved for offline analysis while the owls spontaneously scanned the room and the food items with abrupt gaze shifts (head saccades). From time to time during the experiment, a brief sound was emitted from the speaker. The fixation points immediately following the sounds were extracted and the distances between the gaze position and the nearest items and loudspeaker were measured. The head saccades were rarely toward the location of the sound source but to salient visual features in the room, such as the door knob or the food items. However, among the food items, the one closest to the loudspeaker had the highest probability of attracting a gaze shift. This result supports the notion that auditory signals are integrated with visual information for the selection of the next visual search target.
PMCID: PMC4327738  PMID: 25762905
saliency; saccades; multisensory; visual search; barn owls; selective attention; sound localization
2.  Coding space-time stimulus dynamics in auditory brain maps 
Sensory maps are often distorted representations of the environment, where ethologically-important ranges are magnified. The implication of a biased representation extends beyond increased acuity for having more neurons dedicated to a certain range. Because neurons are functionally interconnected, non-uniform representations influence the processing of high-order features that rely on comparison across areas of the map. Among these features are time-dependent changes of the auditory scene generated by moving objects. How sensory representation affects high order processing can be approached in the map of auditory space of the owl's midbrain, where locations in the front are over-represented. In this map, neurons are selective not only to location but also to location over time. The tuning to space over time leads to direction selectivity, which is also topographically organized. Across the population, neurons tuned to peripheral space are more selective to sounds moving into the front. The distribution of direction selectivity can be explained by spatial and temporal integration on the non-uniform map of space. Thus, the representation of space can induce biased computation of a second-order stimulus feature. This phenomenon is likely observed in other sensory maps and may be relevant for behavior.
PMCID: PMC3986518  PMID: 24782781
sound localization; adaptation; center-surround; acoustic motion; direction selectivity; maps
3.  Saliency mapping in the optic tectum and its relationship to habituation 
Habituation of the orienting response has long served as a model system for studying fundamental psychological phenomena such as learning, attention, decisions, and surprise. In this article, we review an emerging hypothesis that the evolutionary role of the superior colliculus (SC) in mammals or its homolog in birds, the optic tectum (OT), is to select the most salient target and send this information to the appropriate brain regions to control the body and brain orienting responses. Recent studies have begun to reveal mechanisms of how saliency is computed in the OT/SC, demonstrating a striking similarity between mammals and birds. The saliency of a target can be determined by how different it is from the surrounding objects, by how different it is from its history (that is habituation) and by how relevant it is for the task at hand. Here, we will first review evidence, mostly from primates and barn owls, that all three types of saliency computations are linked in the OT/SC. We will then focus more on neural adaptation in the OT and its possible link to temporal saliency and habituation.
PMCID: PMC3893637  PMID: 24474908
habituation; saliency map; optic tectum; superior colliculus; spatial attention; barn owl; orienting response
4.  Responses of Tectal Neurons to Contrasting Stimuli: An Electrophysiological Study in the Barn Owl 
PLoS ONE  2012;7(6):e39559.
The saliency of visual objects is based on the center to background contrast. Particularly objects differing in one feature from the background may be perceived as more salient. It is not clear to what extent this so called “pop-out” effect observed in humans and primates governs saliency perception in non-primates as well. In this study we searched for neural-correlates of pop-out perception in neurons located in the optic tectum of the barn owl. We measured the responses of tectal neurons to stimuli appearing within the visual receptive field, embedded in a large array of additional stimuli (the background). Responses were compared between contrasting and uniform conditions. In a contrasting condition the center was different from the background while in the uniform condition it was identical to the background. Most tectal neurons responded better to stimuli in the contrsating condition compared to the uniform condition when the contrast between center and background was the direction of motion but not when it was the orientation of a bar. Tectal neurons also preferred contrasting over uniform stimuli when the center was looming and the background receding but not when the center was receding and the background looming. Therefore, our results do not support the hypothesis that tectal neurons are sensitive to pop-out per-se. The specific sensitivity to the motion contrasting stimulus is consistent with the idea that object motion and not large field motion (e.g., self-induced motion) is coded in the neural responses of tectal neurons.
PMCID: PMC3380014  PMID: 22745787
5.  The representation of sound localization cues in the barn owl's inferior colliculus 
The barn owl is a well-known model system for studying auditory processing and sound localization. This article reviews the morphological and functional organization, as well as the role of the underlying microcircuits, of the barn owl's inferior colliculus (IC). We focus on the processing of frequency and interaural time (ITD) and level differences (ILD). We first summarize the morphology of the sub-nuclei belonging to the IC and their differentiation by antero- and retrograde labeling and by staining with various antibodies. We then focus on the response properties of neurons in the three major sub-nuclei of IC [core of the central nucleus of the IC (ICCc), lateral shell of the central nucleus of the IC (ICCls), and the external nucleus of the IC (ICX)]. ICCc projects to ICCls, which in turn sends its information to ICX. The responses of neurons in ICCc are sensitive to changes in ITD but not to changes in ILD. The distribution of ITD sensitivity with frequency in ICCc can only partly be explained by optimal coding. We continue with the tuning properties of ICCls neurons, the first station in the midbrain where the ITD and ILD pathways merge after they have split at the level of the cochlear nucleus. The ICCc and ICCls share similar ITD and frequency tuning. By contrast, ICCls shows sigmoidal ILD tuning which is absent in ICCc. Both ICCc and ICCls project to the forebrain, and ICCls also projects to ICX, where space-specific neurons are found. Space-specific neurons exhibit side peak suppression in ITD tuning, bell-shaped ILD tuning, and are broadly tuned to frequency. These neurons respond only to restricted positions of auditory space and form a map of two-dimensional auditory space. Finally, we briefly review major IC features, including multiplication-like computations, correlates of echo suppression, plasticity, and adaptation.
PMCID: PMC3394089  PMID: 22798945
sound localization; central nucleus of the inferior colliculus; auditory; plasticity; adaptation; interaural time difference; interaural level difference; frequency tuning

Results 1-5 (5)